Neotropical Monogenoidea. 56. New species of Anacanthorus

FOLIA PARASITOLOGICA 57[3]: 164–168, 2010
© Institute of Parasitology, Biology Centre ASCR
http://www.paru.cas.cz/folia/
ISSN 0015-5683 (print), ISSN 1803-6465 (online)
Neotropical Monogenoidea. 56. New species of Anacanthorus
(Dactylogyridae) from the gills of matrinchã, Brycon orthotaenia
(Characiformes: Characidae), in the Rio São Francisco, Brazil
Cassandra M. Monteiro1, Delane C. Kritsky2 and Marilia C. Brasil-Sato3
1
Curso de Pós-Graduação em Ciências Veterinárias, Universidade Federal Rural do Rio de Janeiro, Seropédica, Rio de Janeiro,
23890-000, Brazil;
2
Department of Health and Nutrition Sciences, Campus Box 8090, Idaho State University, Pocatello, Idaho 83209, USA;
3
Departamento de Biologia Animal, Universidade Federal Rural do Rio de Janeiro, Km 7, Br 465, CP 74539, Seropédica, Rio de
Janeiro, 23851-970, Brazil
Abstract: Anacanthorus franciscanus sp. n. and Anacanthorus brevicirrus sp. n. (Dactylogyridae) are described from the gills of the
matrinchã, Brycon orthotaenia Günther (Characidae), from the Rio São Francisco in Brazil. Anacanthorus franciscanus most closely
resembles Anacanthorus elegans and A. kruidenieri from the matrinchão, Brycon melanopterus, of the Amazon River Basin. It differs from these species in part by having the bulbous proximal end of the hook shank with two translucent regions. Anacanthorus
brevicirrus resembles A. franciscanus, A. kruidenieri and A. elegans but is differentiated from these species by its short straight male
copulatory organ and by having one translucent region in the bulbous base of the hook shank.
Keywords: Monogenoidea, Dactylogyridae, Anacanthorus, Anacanthorus brevicirrus, Anacanthorus franciscanus,
Brycon orthotaenia, Rio São Francisco, Brazil
The present study is a continuation of ongoing surveys
by personnel of the Universidade Federal Rural do Rio de
Janeiro documenting the diversity of parasites infecting
the fishes of the Rio São Francisco Basin in Brazil (see
Brasil-Sato 2003). In this paper, two new species of Anacanthorus Mizelle et Price, 1965 (Dactylogyridae) are described from the matrinchã, Brycon orthotaenia Günther,
a commercially important characiform fish that is currently threatened with extinction in some reaches of the river
basin (Lins et al. 1997, Sato 1999). The following species
of Monogenoidea have previously been recorded from
Brycon spp.: Anacanthorus brevis Mizelle et Kritsky,
1969, Anacanthorus elegans Kritsky, Thatcher et Kayton,
1979, Anacanthorus kruidenieri Kritsky, Thatcher et Kayton, 1979, Anacanthorus spiralocirrus Kritsky, Thatcher
et Kayton, 1979, Jainus amazonensis Kritsky, Thatcher et
Kayton, 1980 and Tereancistrum kerri Kritsky, Thatcher
et Kayton, 1980 (all Dactylogyridae) from matrichão,
Brycon melanopterus (Cope) (Mizelle and Kritsky 1969,
Kritsky et al. 1979, 1980); Anacanthocotyle sp. (Gyrodactylidae) from Brycon americanus peruanus (host not in
FishBase) (Jara 1986); Annulotrematoides bryconi Cuglianna, Cordeiro et Luque, 2003 (Dactylogyridae) from
matrinchã, Brycon cephalus (Günther) (Cuglianna et al.
2003); Rhinoxenus anaclaudiae Domingues et Boeger,
2005 (Dactylogyridae) from Brycon sp. (Domingues and
Boeger 2005); and Mazocraeoides sp. (Mazocraeidae)
from machaca, Brycon quatemalensis Regen (Fucugauchi-Suarez et al. 1988).
MATERIALS AND METHODS
Specimens of matrinchã were collected from the upper Rio
São Francisco near the municipality of Três Marias (18°12′32″S,
45°15′41″W), State of Minas Gerais, Brazil, by professional
fisherman during July, 2009. Methods of collection and preparation of helminths for study were those of Monteiro et al.
(2010). Measurements, all in micrometres (μm), are the greatest
straight-line distances between extreme points (i.e., distances
along curves are not included in the dimension) and are presented as the mean followed by the range and number (n) of specimens measured in parentheses; body length included that of
the haptor. Type specimens were deposited in the United States
National Parasite Collection, Beltsville, Maryland, USA (USNPC), the Coleção Helmintológica do Instituto Oswaldo Cruz,
Rio de Janeiro, Brazil (CHIOC), and the helminth collections
of the Instituto Nacional de Pesquisas da Amazônia, Manaus,
Amazonas, Brazil (INPA) and of the Institute of Parasitology,
Academy of Sciences of the Czech Republic, České Budějovice,
Czech Republic (IPCAS) as indicated in the respective descriptions. Voucher specimens of the host were deposited in the Museu de Zoologia, Universidade de São Paulo, São Paulo, Brazil
(MZUSP 95166).
Address for correspondence: D.C. Kritsky, Campus Box 8090, Idaho State University, Pocatello, ID 83209, USA. Phone: 1-208-282-3726;
Fax: 1-208-282-4645; E-mail:[email protected]
164
Monteiro et al.: New Anacanthorus spp. from Brazil
RESULTS
Anacanthorus franciscanus sp. n. Figs. 1–4
Description. Body fusiform, 685 (581–828, n = 12)
long, with narrow cephalic region, broad peduncle, bilobed haptor; greatest body width 95 (78–135, n = 12)
at level of male copulatory organ (MCO). Two terminal,
2 bilateral cephalic lobes well developed; terminal lobes
appearing as single lobe when extended. Head organs
usually indistinct; cephalic glands not observed. Four
eyespots; members of posterior pair slightly farther apart,
larger than those of anterior pair; chromatic granules
small, subspherical to ovate; few accessory granules scattered in cephalic region. Pharynx subspherical, 34 (29–44,
n = 10) wide; oesophagus elongate. Haptor 66 (51–107,
n = 11) long, 80 (50–105, n = 12) wide; haptoral lobes
well developed. Hooks similar in size and shape; each 34
(31–36, n = 13) long, with proximal bulbous base containing 2 translucent regions, elongate slender shank, reduced
thumb, evenly curved shaft and open point; filamentous
hook (FH) loop about 1/4 shank length. Single pair of
4As, each 12 (10–14, n = 2) long, with slight proximal
expansion. Gonads tandem or slightly overlapping, intercaecal, lying in posterior half of trunk; testis ovate, 120
(98–152, n = 6) long, 30 (20–45, n = 6) wide; germarium
pyriform, 62 (51–78, n = 7) long, 32 (20–42, n = 6) wide.
Distal portion of uterus weakly sclerotized; vitellaria
comprising 2 bilateral bands of follicles coextensive with
oesophagus and intestine; bands confluent at oesophageal level and posterior to gonads; transverse vitelline
duct immediately anterior to germarium; vagina absent.
MCO 99 (93–107, n = 9) long (from the base to recurve),
a long tube lacking developed base, with recurve (reflex)
at about 2/3 distance to distal flared tip. Accessory piece
45 (40–51, n = 9) long, a membranous sheath covering
about 1/2 proximal portion of MCO between the base and
recurve. Seminal vesicle a simple elongate slight dilation
of vas deferens; prostatic reservoir posterior to base of
MCO on body midline.
T y p e h o s t a n d l o c a l i t y : Matrinchã, Brycon orthotaenia Günther – Rio São Francisco near Três Marias, State
of Minas Gerais, Brazil (18°12′32″S, 45°15′41″W); 19 July
2009.
S i t e o f i n f e c t i o n : Gills.
S p e c i m e n s s t u d i e d : Holotype, CHIOC 37330; 21 paratypes, CHIOC 37331a–e, 37332, INPA 524a–f, USNPC
102884, IPCAS M-507.
E t y m o l o g y : The specific name refers to the Rio São Francisco from which the helminth was collected.
Remarks. The basic morphology of the MCO and
haptoral hooks of A. franciscanus closely resembles that
of Anacanthorus elegans and Anacanthorus kruidenieri
from the matrinchão, Brycon melanopterus, occurring in
the Amazon River drainage. Anacanthorus franciscanus
is differentiated from the latter two species by the reflex
of the MCO occurring at about 2/3 the length from its
base (reflex about 1/2 the distance in A. elegans; near the
distal tip in A. kruidenieri) and by having two translucent
regions in the bulbous base of the hook shank (bulbous
base small and lacking translucence in A. elegans; base
large with one translucent region in A. kruidenieri). Anacanthorus franciscanus differs further from A. kruidenieri
by having a membranous accessory piece in the copulatory complex (accessory piece rod-shaped in A. kruidenieri) (see Kritsky et al. 1979).
Anacanthorus brevicirrus sp. n.
Figs. 5–8
Description. Body fusiform, 590 (476–659, n = 4)
long, with broad cephalic region, short tapered peduncle,
bilobed haptor; greatest body width 79 (64–100, n = 4)
usually posterior to testis. Terminal, 2 bilateral cephalic
lobes well developed; terminal lobe may appear double.
Three pairs of head organs. Postpharyngeal cephalic
glands indistinct, posterolateral to pharynx; prepharyngeal cephalic glands usually visible anterior to eyespots.
Four eyespots; members of posterior pair usually slightly
farther apart or equidistant, larger than those of anterior
pair; chromatic granules small, subspherical to ovate; few
accessory granules scattered in cephalic region. Pharynx
subspherical, 28 (22–32, n = 3) wide; oesophagus elongate. Haptor 45 (30–58, n = 4) long, 64 (55–70, n = 4)
wide; haptoral lobes well developed. Hooks similar in
size and shape; each 35 (31–37, n = 20) long, with small
proximal bulbous base containing translucent spot, elongate slender shank, reduced thumb, nearly straight shaft,
open point; FH loop about 1/2 shank length. Single pair
of 4As, each 10 (9–13, n = 6) long. Gonads tandem or
slightly overlapping, intercaecal, lying in posterior half
of trunk; testis ovate, 57 (47–67, n = 2) long, 27 (18–36,
n = 2) wide; germarium pyriform, 79 (58–118, n = 4) long,
32 (24–48, n = 4) wide. Distal portion of uterus weakly
sclerotized (if at all); vitellaria comprising 2 bilateral
bands of follicles coextensive with oesophagus and intestine; bands confluent at oesophageal level and posterior to
testis; transverse vitelline duct anterior to germarium; vagina absent. MCO 36 (30–41, n = 10) long, a short broad
tube lacking developed base. Accessory piece 16 (11–22,
n = 8) long, a membranous tape-like structure partially
encircling distal half of MCO. Seminal vesicle a simple
elongate dilation of vas deferens; small prostatic reservoir
posterior to base of MCO.
T y p e h o s t a n d l o c a l i t y : Matrinchã, Brycon orthotaenia Günther – Rio São Francisco near Três Marias, State
of Minas Gerais, Brazil (18°12′32″S, 45°15′41″W); 19 July
2009.
S i t e o f i n f e c t i o n : Gills.
S p e c i m e n s s t u d i e d : Holotype, CHIOC 37333a;
13 paratypes, CHIOC 37333b, c, 37334, INPA 523a–c, USNPC 102883, IPCAS M-508.
165
30
200
5
200
3
6
7
4
1
2
8
Figs. 1–8. Anacanthorus spp. from the matrinchã, Brycon orthotaenia, from the Rio São Francisco, Brazil. Figs. 1–4. Anacanthorus franciscanus sp. n. Fig. 1. Whole mount (ventral view, composite). Fig. 2. Copulatory complex (ventral view). Fig. 3. 4A.
Fig. 4. Hook. Figs. 5–8. Anacanthorus brevicirrus sp. n. Fig. 5. Copulatory complex (ventral view). Fig. 6. Hook. Fig. 7. 4A.
Fig. 8. Whole mount (ventral, composite). Figs. 1 and 8 are presented to the respective 200 μm scales; Figs. 2–7 are to the 30 μm
scale.
E t y m o l o g y : The specific name is from Latin [brevi = short,
cirrus = a curl (of hair)] and refers to the MCO.
Remarks. Based on the comparative morphology of
the hooks, A. brevicirrus apparently shares an evolutionary history with A. elegans, A. franciscanus and A. kruidenieri, all of which are parasites of species of Brycon.
166
Anacanthorus brevicirrus is easily differentiated from the
latter three species by having a short straight MCO (MCO
elongate, with recurve in latter three species). Among
species of Anacanthorus, only A. euryphallus Kritsky,
Boeger et Van Every, 1992 from Triportheus spp. (Characidae) possesses a MCO comprising a broad short tube
Monteiro et al.: New Anacanthorus spp. from Brazil
similar to that of A. brevicirrus. However, the accessory
piece of A. euryphallus is a branched rod, while that of
A. brevicirrus is membranous (see Kritsky et al. 1992).
DISCUSSION
Anacanthorus currently includes 63 species from the
gills of Neotropical characiform fishes (Thatcher 2006)
and is primarily characterized by dactylogyrids lacking
a vagina and haptoral anchor/bar complexes (Kritsky et
al. 1992). The genus was established by Mizelle and Price
(1965) for three species from the gills of a red piranha,
Serrasalmus nattereri Kner [now Pygocentrus nattereri
Kner] (Serrasalmidae), held in the Steinhart Aquarium
in San Francisco, California. Of the 42 valid species of
Brycon (see Froese and Pauly 2009), only the matrinchão, B. melanopterus from the Amazon Basin, has been
previously documented as a host for species of the genus
(Mizelle and Kritsky 1969, Kritsky et al. 1979).
All previously described species of Anacanthorus
are from fishes of the Amazon River Basin, except Anacanthorus penilabiatus Boeger, Husak et Martins, 1995,
which was originally described from Piaractus mesopotamicus (Holmberg) (Serrasalmidae) cultivated in the
State of São Paulo, Brazil (Boeger et al. 1995). Anacanthorus penilabiatus has subsequently been reported from
P. mesopotamicus, Piaractus brachypomum (Cuvier) and
Colossoma macropomum (Cuvier) (all Serrasalmidae),
maintained in fish ponds in the Brazilian states of Ceará
and São Paulo (Pamplona-Basilio et al. 2001, among others). Cohen and Kohn (2009) also reported A. penilabiatus on P. mesopotamicus from outside the Amazon Basin,
but it is unclear from the presentation of the results of
their study whether or not the helminth occurred in a natural habitat (Itaipu Hydroelectric Power Station Reservoir
on the Paraná River). Finally, Santos (2008) and Albuquerque (2009) recorded unidentified species of Anacanthorus from the gills of Pygocentrus piraya (Cuvier) and
Serrasalmus brandtii Lütken (both Serrasalmidae) and
Triportheus guentheri (Garman) (Characidae) from the
Rio São Francisco drainage, respectively. Thus, A. franciscanus and A. brevicirrus from the Rio São Francisco
are the first identified and described members of the genus clearly recorded from a natural habitat outside of the
Amazon Basin.
The Rio São Francisco drainage in Brazil shares diverse biological components with those of other river
systems in South America (Hubert and Renno 2006). For
example, of eight dactylogyrid species occurring on the
gills of the catfish, Pimelodus maculatus Lacépède, in
the Rio São Francisco Basin, only two, Demidospermus
ichthyocercus Monteiro, Kritsky et Brasil-Sato, 2010 and
Ameloblastella satoi Monteiro, Kritsky et Brasil-Sato,
2010, are currently restricted to this river system (Monteiro et al. 2010); the remaining six dactylogyrid species
on this host also occur in the Platina (Paraná) Drainage of
Brazil and Argentina (Kritsky and Gutiérrez 1998, Cohen
and Kohn 2008, Santos et al. 2007). The biogeographical
explanation for the distributions of these dactylogyrids is
in part confounded because of natural and artificial watershed transpositions that have occurred between the Rio
São Francisco and the Platina basins (Filho and Buckup
2005) which might have allowed parasite dispersal between the two river systems. Thus, both vicariance and
dispersal are likely required to explain extant distributions
of these parasites.
The present study suggests that a vicariance/coevolutionary model might be responsible for A. franciscanus and A. brevicirrus on B. orthotaenia in the Rio São
Francisco. These parasite species are morphologically
similar to A. kruidenieri, A. brevis and A. elegans from
B. melanopterus from the Amazon River, suggesting that
a common ancestor existed for the five dactylogyrid species. Supporting this are the morphological characteristics
of the haptoral hooks (straight open point and shaft and
presence of translucent regions in the base of the shaft)
and copulatory complex (broad tubular MCO and presence of a membranous accessory piece in four of the five
species) and the apparent restricted distributions of the respective hosts and their Anacanthorus spp. in the two river systems. In addition, the morphological features of the
species of Anacanthorus from Brycon spp. are not shared
with any other members of Anacanthorus from unrelated
hosts and may represent derived synapomorphic characters that might signal the presence of a monophyletic lineage within the genus (see Kritsky et al. 1992).
Acknowledgements. Dr. Yoshimi Sato, leader of the EPT/
CODEVASF, Três Marias, Minas Gerais, CEMIG-GT/
CODEVASF and UFRRJ/IBAMA, Minas Gerais, is gratefully
acknowledged for providing logistical and material support during collections of hosts. CMM was supported by a student fellowship from CAPES (Bex 0750-09-3).
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